Positive and negative peptide signals control stomatal density

Abstract

The stoma is a micro valve found on aerial plant organs that promotes gas exchange between the atmosphere and the plant body. Each stoma is formed by a strict cell lineage during the early stages of leaf development. Molecular genetics research using the model plant Arabidopsis has revealed the genes involved in stomatal differentiation. Cysteine-rich secretory peptides of the EPIDERMAL PATTERNING FACTOR-LIKE (EPFL) family play crucial roles as extracellular signaling factors. Stomatal development is orchestrated by the positive factor STOMAGEN/EPFL9 and the negative factors EPF1, EPF2, and CHALLAH/EPFL6 in combination with multiple receptors. EPF1 and EPF2 are produced in the stomatal lineage cells of the epidermis, whereas STOMAGEN and CHALLAH are derived from the inner tissues. These findings highlight the complex cell-to-cell and intertissue communications that regulate stomatal development. To optimize gas exchange, particularly the balance between the uptake of carbon dioxide (CO(2)) and loss of water, plants control stomatal activity in response to environmental conditions. The CO(2) level and light intensity influence stomatal density. Plants sense environmental cues in mature leaves and adjust the stomatal density of newly forming leaves, indicating the involvement of long-distance systemic signaling. This review summarizes recent research progress in the peptide signaling of stomatal development and discusses the evolutionary model of the signaling machinery.

Fig. 1

Stomatal development and cell-to-cell signaling in the Arabidopsis leaf. During leaf development, the protodermal cell differentiates into either a guard cell (GC) or a pavement cell. Three paralogous bHLH transcription factors, SPEECHLESS (SPCH), MUTE, and FAMA, regulate the progression of the stomatal lineage sequentially. SPCH regulates the differentiation of protodermal cells to meristemoid mother cells (MMCs). Subsequently, entry division begins to produce stomatal lineage ground cells (SLGCs) and a meristemoid (M), which is differentiated into the guard mother cell (GMC) by MUTE. FAMA regulates the symmetric division of GMC to produce GCs (i.e., a stoma). Stomatal development is regulated by cell-to-cell communication through signaling peptides including stomagen, EPF1, and EPF2. Stomagen, which is derived from internal tissues, positively regulates stomatal development at several steps as indicated. EPF2 is produced mainly in the MMC to inhibit the differentiation of protodermal cells into an MMC, whereas EPF1 is produced mainly in the GMC to inhibit the differentiation of the M into a GMC. EPF1 also regulates the direction of the spacing division to produce the satellite meristemoid (SM)

Fig. 2

The EPFL family of signaling peptides in Arabidopsis. a Schematic illustration of the domain structure of STOMAGEN/EPFL9, which is composed of the signal peptide (SP), the N-terminal propeptide (NTPP), and the mature domain. Amino acid positions are indicated above the structure. b Amino acid sequence alignment of putative mature domains of the EPFL family. Identical amino acid residues are shaded in blue. Conserved cysteine residues (C) are shaded in red. Three disulfide bridges of stomagen are indicated by solid lines. The putative pairs of additional cysteine residues are linked by a dotted line. Sequences are aligned by Clustal W. c Phylogenetic tree of the EPFL family. Bootstrap values for 1,000 replications are indicated on each node. The phylogenetic tree is constructed by a neighbor-joining method using the alignment in b with MEGA version 4 software [49]

Fig. 3

A model of the peptide signaling system during stomatal development. Stomatal development is promoted by transcription factors (TFs) in the absence of peptide signaling and MAPK cascade. ERf and TMM form the negative receptor complex at the plasma membrane. The negative signaling peptide EPFs and the positive signaling peptide stomagen interact competitively with the receptor complex. The kinase domain of ERf transmits negative signals to the MAPK cascade, which represses the function of TFs. The molecular function of the negative factor SDD1 is unknown

Fig. 4

Systemic signaling for stomatal development in response to environmental conditions. The mature leaf perceives environmental cues, such as light intensity or CO₂ level, to generate an unknown systemic signal (X). The systemic signal migrates to the leaf primordium, which alters stomatal density on the developing leaf

Fig. 5

An evolutionary model of the signaling machinery of stomatal development. a A possible ancestral signaling system in stomatal development. Stomatal development is promoted by the transcription factor (TF). The negative signaling peptide (NP) is perceived by the cell-surface receptor complex (RC), which represses the function of the TF. b Duplication of the signaling peptide. The positive signaling peptide (PP) may be generated by gene duplication of NP and subsequent conversion of negative activity to positive activity. The PP may bind competitively to the RC, but it loses signal transmission activity. c Duplication of the signaling system resulting in multiple steps of stomatal development. Each of the regulatory factors, NP, RC, and TF, is duplicated and subsequently acquires a distinct function. Stomagen is the only known PP so far